Although the vinegar fly Drosophila melanogaster isarguably the most studied organism on the planet,fundamental aspects of this species’ natural ecologyhave remained enigmatic [1]. We have here investigateda wild population of D. melanogaster from amopane forest in Zimbabwe. We find that these fliesare closely associated with marula fruit (Sclerocaryabirrea) and propose that this seasonally abundantand predominantly Southern African fruit is a keyancestral host of D. melanogaster. Moreover, whenfruiting, marula is nearly exclusively used byD. melanogaster, suggesting that these forest-dwellingD. melanogaster are seasonal specialists, in asimilar manner to, e.g., Drosophila erecta on screwpine cones [2]. We further demonstrate that themain chemicals released by marula activate odorantreceptors that mediate species-specific host choice(Or22a) [3, 4] and oviposition site selection (Or19a)[5]. The Or22a-expressing neurons—ab3A—respondstrongly to the marula ester ethyl isovalerate, a volatilerarely encountered in high amounts in other fruit.We also show that Or22a differs among African populationssampled from a wide range of habitats, inline with a function associated with host fruit usage.Flies from Southern Africa, most of which carry adistinct allele at the Or22a/Or22b locus, have ab3Aneurons that are more sensitive to ethyl isovaleratethan, e.g., European flies. Finally, we discuss thepossibility that marula, which is also a culturallyand nutritionally important resource to humans,may have helped the transition to commensalism inD. melanogaster
